Calcium prevents retinoic acid-induced disruption of the spectrin-based cytoskeleton in keratinocytes through the Src/PI3K-p85α/AKT/PKCδ/β-adducin pathways

Cell Calcium

Volumn 54, Issue 3, 2013, Pages 151-162

  Zhao, Kong Nan ^a,b   Masci, Paul P ^a   Chen, Jiezhong ^a   Lavin, Martin F ^b,c  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

Adducin; AKT; Calcium; Keratinocyte differentiation; PI3K; PKC ; Retinoic acid; Spectrin based cytoskeleton; Src

Indexed keywords

ADDUCIN; BETA ADDUCIN; CALCIUM; CYCLIN B1; CYCLIN D2; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN KINASE C DELTA; PROTEIN P85; PROTEIN TYROSINE KINASE; RETINOIC ACID; SERINE; SPECTRIN; THREONINE; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOSKELETON; DOWN REGULATION; EXTRACELLULAR CALCIUM; INHIBITION KINETICS; KERATINOCYTE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION;

ADDUCIN; AKT; CALCIUM; KERATINOCYTE DIFFERENTIATION; PI3K; PKCΔ; RETINOIC ACID; SPECTRIN-BASED CYTOSKELETON; SRC;

ANIMALS; CALCIUM; CALMODULIN-BINDING PROTEINS; CELL DIFFERENTIATION; CELLS, CULTURED; CLASS IA PHOSPHATIDYLINOSITOL 3-KINASE; CYCLIN D2; CYTOSKELETON; GENE EXPRESSION; KERATINOCYTES; MICE; PHOSPHORYLATION; PROTEIN KINASE C BETA; PROTEIN KINASE C-DELTA; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SPECTRIN; SRC-FAMILY KINASES; TRETINOIN; UP-REGULATION;

EID: 84883250877     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2013.05.009     Document Type: Article

References (80)

1. Toulza E., Mattiuzzo N.R., Galliano M.F., Jonca N., Dossat C., et al. Large-scale identification of human genes implicated in epidermal barrier function. Genome Biology 2007, 8:R107.
2. Fuchs E., Raghavan S. Getting under the skin of epidermal morphogenesis. Nature Reviews Genetics 2002, 3:199-209.
3. Eckert R.L., Crish J.F., Robinson N.A. The epidermal keratinocyte as a model for the study of gene regulation and cell differentiation. Physiological Reviews 1997, 77:397-424.
4. Fuchs E. Scratching the surface of skin development. Nature 2007, 445:834-842.
5. Metral S., Machnicka B., Bigot S., Colin Y., Dhermy D., et al. AlphaII-spectrin is critical for cell adhesion and cell cycle. Journal of Biological Chemistry 2009, 284:2409-2418.
6. de Cuevas M., Lee J.K., Spradling A.C. Alpha-spectrin is required for germline cell division and differentiation in the Drosophila ovary. Development 1996, 122:3959-3968.
7. Lee J.K., Brandin E., Branton D., Goldstein L.S. alpha-Spectrin is required for ovarian follicle monolayer integrity in Drosophila melanogaster. Development 1997, 124:353-362.
8. Mishra L., Cai T., Yu P., Monga S.P., Mishra B. Elf3 encodes a novel 200-kD beta-spectrin: role in liver development. Oncogene 1999, 18:353-364.
9. Kim S.S., Shetty K., Katuri V., Kitisin K., Baek H.J., et al. TGF-beta signaling pathway inactivation and cell cycle deregulation in the development of gastric cancer: role of the beta-spectrin, ELF. Biochemical and Biophysical Research Communications 2006, 344:1216-1223.
10. Kariniemi A.L., Lehto V.P., Virtanen I. Distribution of p230, an alpha-spectrin-related polypeptide in normal and psoriatic epidermis and in cultured human keratinocytes. British Journal of Dermatology 1984, 111:139-145.
11. Tuominen H., Sormunen R., Kallioinen M. Non-erythroid spectrin (fodrin) in cutaneous tumours: diminished in cell membranes, increased in the cytoplasm. British Journal of Dermatology 1996, 135:576-580.
12. De G.V., Sestini S., Massi D., Panelos J., Papi F., et al. Subungual melanoma: a particularly invasive onychomycosis. Journal of the American Geriatrics Society 2007, 55:2094-2096.
13. Rizzuto R., Pozzan T. When calcium goes wrong: genetic alterations of a ubiquitous signaling route. Nature Genetics 2003, 34:135-141.
14. de G.V., Sestini S., Massi D., Ghersetich I., Lotti T. Keratinocyte growth factor receptors. Dermatologic clinics 2007, 25:477-485. vii.
15. Juliandi B., Abematsu M., Nakashima K. Chromatin remodeling in neural stem cell differentiation. Current opinion in neurobiology 2010, 20:408-415.
16. de G.V., Sestini S., Massi D., Lotti T. Melanocytic aggregation in the skin: diagnostic clues from lentigines to melanoma. Dermatologic clinics 2007, 25:303-320. vii-viii.
17. Yuspa S.H., Hennings H., Tucker R.W., Jaken S., Kilkenny A.E., et al. Signal transduction for proliferation and differentiation in keratinocytes. Annals of the New York Academy of Sciences 1988, 548:191-196.
18. Behne M.J., Jensen J.M. Calcium in epidermis. Advances in experimental medicine and biology 2012, 740:945-953.
19. Cornelissen L.H., Oomens C.W., Huyghe J.M., Baaijens F.P. Mechanisms that play a role in the maintenance of the calcium gradient in the epidermis. Skin Research and Technology: Official Journal of International Society for Bioengineering and the Skin 2007, 13:369-376.
20. Leinonen P.T., Hagg P.M., Peltonen S., Jouhilahti E.M., Melkko J., et al. Reevaluation of the normal epidermal calcium gradient, and analysis of calcium levels and ATP receptors in Hailey-Hailey and Darier epidermis. Journal of Investigative Dermatology 2009, 129:1379-1387.
21. Hennings H., Michael D., Cheng C., Steinert P., Holbrook K., et al. Calcium regulation of growth and differentiation of mouse epidermal cells in culture. Cell 1980, 19:245-254.
22. Fang N.X., Gu W., Ding J., Saunders N.A., Frazer I.H., et al. Calcium enhances mouse keratinocyte differentiation in vitro to differentially regulate expression of papillomavirus authentic and codon modified L1 genes. Virology 2007, 365:187-197.
23. Marcelo C.L., Kim Y.G., Kaine J.L., Voorhees J.J. Stratification, specialization, and proliferation of primary keratinocyte cultures. Evidence of a functioning in vitro epidermal cell system. Journal of Cell Biology 1978, 79:356-370.
24. Juliandi B., Abematsu M., Nakashima K. Epigenetic regulation in neural stem cell differentiation. Development, Growth and Differentiation 2010, 52:493-504.
25. Cvekl A., Wang W.L. Retinoic acid signaling in mammalian eye development. Experimental eye research 2009, 89:280-291.
26. Mark M., Ghyselinck N.B., Chambon P. Function of retinoic acid receptors during embryonic development. Nuclear Receptor Signaling 2009, 7:e002.
27. Napoli J.L. Physiological insights into all-trans-retinoic acid biosynthesis. Biochimica et biophysica acta 2012, 1821:152-167.
28. Li B., Wang X., Zhou F., Saunders N.A., Frazer I.H., et al. Up-regulated expression of Sp1 protein coincident with a viral protein in human and mouse differentiating keratinocytes may act as a cell differentiation marker. Differentiation 2008, 76:1068-1080.
29. Danilenko M., Wang X., Studzinski G.P. Carnosic acid and promotion of monocytic differentiation of HL60-G cells initiated by other agents. Journal of the National Cancer Institute 2001, 93:1224-1233.
30. Moon R.C., Mehta R.G., Detrisac C.J. Retinoids as chemopreventive agents for breast cancer. Cancer Detection and Prevention 1992, 16:73-79.
31. Mandili G., Marini C., Carta F., Zanini C., Prato M., et al. Identification of phosphoproteins as possible differentiation markers in all-trans-retinoic acid-treated neuroblastoma cells. PLoS ONE 2011, 6:e18254.
32. Morizane S., Yamasaki K., Kabigting F.D., Gallo R.L. Kallikrein expression and cathelicidin processing are independently controlled in keratinocytes by calcium, vitamin D(3), and retinoic acid. Journal of Investigative Dermatology 2010, 130:1297-1306.
33. Larsen F.G., Voorhees J.J., Astrom A. Retinoic acid induces expression of early growth response gene-1 (Egr-1) in human skin in vivo and in cultured skin fibroblasts. Journal of Investigative Dermatology 1994, 102:730-733.
34. Zhao K.N., Masci P.P., Lavin M.F. Disruption of spectrin-like cytoskeleton in differentiating keratinocytes by PKCdelta activation is associated with phosphorylated adducin. PLoS ONE 2011, 6:e28267.
35. Zhao Y., Sudol M., Hanafusa H., Krueger J. Increased tyrosine kinase activity of c-Src during calcium-induced keratinocyte differentiation. Proceedings of the National Academy of Sciences of the United States of America 1992, 89:8298-8302.
36. Zhao K.N., Gu W., Fang N.X., Saunders N.A., Frazer I.H. Gene codon composition determines differentiation-dependent expression of a viral capsid gene in keratinocytes in vitro and in vivo. Molecular and Cellular Biology 2005, 25:8643-8655.
37. 2+ on human skin in organ culture. American Journal of Pathology 1993, 142:189-198.
38. Varani J., Perone P., Fligiel S.E., Inman D.R., Voorhees J.J. All-trans-retinoic acid preserves viability of fibroblasts and keratinocytes in full-thickness human skin and fibroblasts in isolated dermis in organ culture. Archives of dermatological research 1994, 286:443-447.
39. Tang X.H., Vivero M., Gudas L.J. Overexpression of CRABPI in suprabasal keratinocytes enhances the proliferation of epidermal basal keratinocytes in mouse skin topically treated with all-trans retinoic acid. Experimental cell research 2008, 314:38-51.
40. Hansen L.A., Sigman C.C., Andreola F., Ross S.A., Kelloff G.J., et al. Retinoids in chemoprevention and differentiation therapy. Carcinogenesis 2000, 21:1271-1279.
41. Li E.R., Owens D.M., Djian P., Watt F.M. Expression of involucrin in normal, hyperproliferative and neoplastic mouse keratinocytes. Experimental Dermatology 2000, 9:431-438.
42. Calautti E., Missero C., Stein P.L., Ezzell R.M., Dotto G.P. Fyn tyrosine kinase is involved in keratinocyte differentiation control. Genes and Development 1995, 9:2279-2291.
43. Kuo H.C., Kuo W.H., Lee Y.J., Wang C.J., Tseng T.H. Enhancement of caffeic acid phenethyl ester on all-trans retinoic acid-induced differentiation in human leukemia HL-60 cells. Toxicology and Applied Pharmacology 2006, 216:80-88.
44. Ding J., Doorbar J., Li B., Zhou F., Gu W., et al. Expression of papillomavirus L1 proteins regulated by authentic gene codon usage is favoured in G2/M-like cells in differentiating keratinocytes. Virology 2010, 399:46-58.
45. Blain S.W. Switching cyclin D-Cdk4 kinase activity on and off. Cell Cycle 2008, 7:892-898.
46. Lindqvist A., Rodriguez-Bravo V., Medema R.H. The decision to enter mitosis: feedback and redundancy in the mitotic entry network. Journal of Cell Biology 2009, 185:193-202.
47. Kim S., Coulombe P.A. Emerging role for the cytoskeleton as an organizer and regulator of translation. Nature Reviews Molecular Cell Biology 2010, 11:75-81.
48. Reedy M.V., Faraco C.D., Erickson C.A. Specification and migration of melanoblasts at the vagal level and in hyperpigmented Silkie chickens. Developmental Dynamics: An Official Publication of the American Association of Anatomists 1998, 213:476-485.
49. Eckert R.L., Crish J.F., Efimova T., Dashti S.R., Deucher A., et al. Regulation of involucrin gene expression. Journal of Investigative Dermatology 2004, 123:13-22.
50. Efimova T., Broome A.M., Eckert R.L. Protein kinase Cdelta regulates keratinocyte death and survival by regulating activity and subcellular localization of a p38delta-extracellular signal-regulated kinase 1/2 complex. Molecular and Cellular Biology 2004, 24:8167-8183.
51. Adhikary G., Chew Y.C., Reece E.A., Eckert R.L. PKC-delta and -eta, MEKK-1, MEK-6, MEK-3, and p38-delta are essential mediators of the response of normal human epidermal keratinocytes to differentiating agents. Journal of Investigative Dermatology 2010, 130:2017-2030.
52. Deucher A., Efimova T., Eckert R.L. Calcium-dependent involucrin expression is inversely regulated by protein kinase C (PKC)alpha and PKCdelta. Journal of Biological Chemistry 2002, 277:17032-17040.
53. Whelan R.D., Kiley S.C., Parker P.J. Tetradecanoyl phorbol acetate-induced microtubule reorganization is required for sustained mitogen-activated protein kinase activation and morphological differentiation of U937 cells. Cell Growth and Differentiation 1999, 10:271-277.
54. Mori D., Yamada M., Mimori-Kiyosue Y., Shirai Y., Suzuki A., et al. An essential role of the aPKC-Aurora A-NDEL1 pathway in neurite elongation by modulation of microtubule dynamics. Nature Cell Biology 2009, 11:1057-1068.
55. Baron W., de Vries E.J., de Vries H., Hoekstra D. Protein kinase C prevents oligodendrocyte differentiation: modulation of actin cytoskeleton and cognate polarized membrane traffic. Journal of Neurobiology 1999, 41:385-398.
56. Zhao K.W., Li X., Zhao Q., Huang Y., Li D., et al. Protein kinase Cdelta mediates retinoic acid and phorbol myristate acetate-induced phospholipid scramblase 1 gene expression: its role in leukemic cell differentiation. Blood 2004, 104:3731-3738.
57. Jiang K., Apostolatos A.H., Ghansah T., Watson J.E., Vickers T., et al. Identification of a novel antiapoptotic human protein kinase C delta isoform, PKCdeltaVIII in NT2 cells. Biochemistry 2008, 47:787-797.
58. Kambhampati S., Li Y., Verma A., Sassano A., Majchrzak B., et al. Activation of protein kinase C delta by all-trans-retinoic acid. Journal of Biological Chemistry 2003, 278:32544-32551.
59. Oh Y.I., Kim J.H., Kang C.W. Oxidative stress in MCF-7 cells is involved in the effects of retinoic acid-induced activation of protein kinase C-delta on insulin-like growth factor-I secretion and synthesis. Growth Hormone & IGF Research: Official Journal of the Growth Hormone Research Society and the International IGF Research Society 2010, 20:101-109.
60. del R.S.V., Guo Q., Morelli C., Shiu H.Y., Surmacz E., et al. Retinoic acid mediates degradation of IRS-1 by the ubiquitin-proteasome pathway, via a PKC-dependant mechanism. Oncogene 2004, 23:9269-9279.
61. Gardner K., Bennett V. Modulation of spectrin-actin assembly by erythrocyte adducin. Nature 1987, 328:359-362.
62. Gilligan D.M., Sarid R., Weese J. Adducin in platelets: activation-induced phosphorylation by PKC and proteolysis by calpain. Blood 2002, 99:2418-2426.
63. Xie Z., Singleton P.A., Bourguignon L.Y., Bikle D.D. Calcium-induced human keratinocyte differentiation requires src- and fyn-mediated phosphatidylinositol 3-kinase-dependent activation of phospholipase C-gamma1. Molecular biology of the cell 2005, 16:3236-3246.
64. Gianni M., Parrella E., Raska I., Gaillard E., Nigro E.A., et al. P38MAPK-dependent phosphorylation and degradation of SRC-3/AIB1 and RARalpha-mediated transcription. EMBO Journal 2006, 25:739-751.
65. Chai Z., Yang L., Yu B., He Q., Li W.I., et al. p38 mitogen-activated protein kinase-dependent regulation of SRC-3 and involvement in retinoic acid receptor alpha signaling in embryonic cortical neurons. IUBMB life 2009, 61:670-678.
66. Miranda M.B., Redner R.L., Johnson D.E. Inhibition of Src family kinases enhances retinoic acid induced gene expression and myeloid differentiation. Molecular Cancer Therapeutics 2007, 6:3081-3090.
67. Gianni M., Kopf E., Bastien J., Oulad-Abdelghani M., Garattini E., et al. Down-regulation of the phosphatidylinositol 3-kinase/Akt pathway is involved in retinoic acid-induced phosphorylation, degradation, and transcriptional activity of retinoic acid receptor gamma 2. Journal of Biological Chemistry 2002, 277:24859-24862.
68. Koga F., Xu W., Karpova T.S., McNally J.G., Baron R., et al. Hsp90 inhibition transiently activates Src kinase and promotes Src-dependent Akt and Erk activation. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:11318-11322.
69. Deb D.K., Sassano A., Lekmine F., Majchrzak B., Verma A., et al. Activation of protein kinase C delta by IFN-gamma. Journal of immunology 2003, 171:267-273.
70. Calautti E., Li J., Saoncella S., Brissette J.L., Goetinck P.F. Phosphoinositide 3-kinase signaling to Akt promotes keratinocyte differentiation versus death. Journal of Biological Chemistry 2005, 280:32856-32865.
71. Konishi H., Matsuzaki H., Takaishi H., Yamamoto T., Fukunaga M., et al. Opposing effects of protein kinase C delta and protein kinase B alpha on H(2)O(2)-induced apoptosis in CHO cells. Biochemical and biophysical research communications 1999, 264:840-846.
72. Matsuoka H., Tsubaki M., Yamazoe Y., Ogaki M., Satou T., et al. Tamoxifen inhibits tumor cell invasion and metastasis in mouse melanoma through suppression of PKC/MEK/ERK and PKC/PI3K/Akt pathways. Experimental cell research 2009, 315:2022-2032.
73. Sud N., Wedgwood S., Black S.M. Protein kinase Cdelta regulates endothelial nitric oxide synthase expression via Akt activation and nitric oxide generation. American Journal of Physiology: Lung cellular and Molecular Physiology 2008, 294:L582-L591.
74. Kwon O.S., Pyo H.K., Oh Y.J., Han J.H., Lee S.R., et al. Promotive effect of minoxidil combined with all-trans retinoic acid (tretinoin) on human hair growth in vitro. Journal of Korean medical science 2007, 22:283-289.
75. Wang Z., Song Y., Tu W., He X., Lin J., et al. beta-2 spectrin is involved in hepatocyte proliferation through the interaction of TGFbeta/Smad and PI3K/AKT signalling. Liver International: Official Journal of the International Association for the Study of the Liver 2012, 32:1103-1111.
76. Lin C.H., Lee C.C., Gean P.W. Involvement of a calcineurin cascade in amygdala depotentiation and quenching of fear memory. Molecular pharmacology 2003, 63:44-52.
77. Sasabe E., Tatemoto Y., Li D., Yamamoto T., Osaki T. Mechanism of HIF-1alpha-dependent suppression of hypoxia-induced apoptosis in squamous cell carcinoma cells. Cancer Science 2005, 96:394-402.
78. Dong F., Li Q., Sreejayan N., Nunn J.M., Ren J. Metallothionein prevents high-fat diet induced cardiac contractile dysfunction: role of peroxisome proliferator activated receptor gamma coactivator 1alpha and mitochondrial biogenesis. Diabetes 2007, 56:2201-2212.
79. Macurek L., Lindqvist A., Medema R.H. Aurora-A and hBora join the game of Polo. Cancer Research 2009, 69:4555-4558.
80. Gandarillas A., Davies D., Blanchard J.M. Normal and c-Myc-promoted human keratinocyte differentiation both occur via a novel cell cycle involving cellular growth and endoreplication. Oncogene 2000, 19:3278-3289.